DOI: 10.1111/jbg.
12361
EDITORIAL
The fundamental theorem of natural selection
This is the last editorial celebrating Fisher’s classic and
hugely influential 1918 paper (Trans. R. Soc. Edinburgh 52,
399–433) in its centenary year. Selection was mentioned in
1918 as a possible confounder of measured correlations, but
the main aim was to reconcile biometrics with Mendelism. In
The Genetical Theory of Natural Selection in 1930, however,
Fisher wanted to render mathematically respectable the idea
that natural selection improved organisms and created biolog-
ical design. Fisher had taken with him as an undergraduate to
Cambridge a set of Darwin’s complete works, and through-
out his life wrote eloquently and influentially about the broad
biological (and more controversially social) implications of
Darwinian thinking.
When natural selection became the focus of Fisher’s think-
ing, some of the simplifying assumptions of 1918 became too
simple. In particular, Fisher (1927, Eug. Rev. 19, 103–108)
confronted the complications of age structure in a study of
human life tables and developed the concept of reproductive
value. Each age class was assigned its own numerical value,
which represented relative contributions of typical individ-
uals of the different classes to the asymptotic gene pool. He
went on to develop, for age‐structured populations, the funda-
mental theorem of natural selection as the jewel in the crown
of his 1930 book, namely “The rate of increase in fitness of
any organism at any time is equal to its genetic variance in
fitness at that time” (Fisher, 1930, page 35).
But, what is fitness? Recent work (Grafen, 2015, Am. Nat.
186, 1–14) shows that Fisher’s concept of fitness is not just
“a parameter in a model” (pace Ewens, 2004 Mathematical
Population Genetics I. Theoretical Introduction. Springer).
Each individual has a fitness at each moment in time, not
a single “tombstone” figure. It is convenient to discuss dis-
crete time, as the principles are the same. Using the 1927
per capita class‐based reproductive values, the reproductive
value the individual produces this period comes under two
headings: half of the reproductive value of its expected num-
ber of offspring (age zero), and the individual’s own chance
of survival times her reproductive value (at 1 year older,
of course). This is like the usual Leslie matrix calculation,
except that here it is performed on an individual basis, al-
lowing an individual’s genotype to influence offspring num-
ber and survival. Williams (1966, Am. Nat, 100, 687–690)
founded life‐history theory with this concept, which we will
call “Williams’ reproductive value” to distinguish it from
the 1927 class‐based values. Indeed, if individual i at some
particular moment has Williams’ reproductive value Wi and
J Anim Breed Genet. 2018;135:393–394. wileyonlinelibrary.com/journal/jbg © 2018 Blackwell Verlag GmbH     393
belongs to a class with 1927 value vi, then Fisher’s implicit
definition of its fitness mi at that time is
Wi − vi
mi = ,
vi
which is therefore the proportional advantage an individual
has over the average its age class would have in a static popula-
tion. Fisher’s fitness has a number of remarkable properties: (a)
the mean fitness within each age class is the same; (b) despite
being a weighted sum of reproductive value (“downstairs”), the
mean fitness equals the Malthusian parameter, that is the growth
rate of the population as measured by the Euler–Lotka equation
in its exponent (“upstairs”); and (c) in a population in demo-
graphic equilibrium, the mean fitness is therefore zero. The up-
stairs/downstairs duality lies at the heart of the theory and binds
together evolutionary and ecological concepts of fitness.
A second question is: How can mean fitness always be going
up? Reconciling the non‐negative value from the fundamental
theorem with an ecological necessity of roughly constant fit-
ness turns out to be relatively simple. Fisher was usually clear
that only part of the rate of change equals what we would now
call the additive genetic variance in fitness, namely that part
due to natural selection, and within a dozen pages of the theo-
rem showed he appreciated this second puzzle, by presenting a
model of other components that can, and usually will, leave the
total rate of change at about zero. Fisher preferred brevity over
[i.e. a space to make two words "over" and then "complete-
ness"] completeness in the famous verbal statement, which
may be responsible for the theorem’s evident power to inspire,
but proved to be catastrophic for readers’ understanding of it.
Biologists in traditions inspired by the theorem mainly
cited Hamilton (1964, J. Theor. Biol 7, 1–52) and Williams
(1966, ibid.), who themselves cited Fisher. The shining ex-
ample of mathematical support for this work is the oeuvre of
Charlesworth from 1970 (Theor. Pop. Biol. 1, 352–370) on-
wards (now summarized in Charlesworth, 1994 Evolution in
Age‐Structured Populations, 2nd ed., Cambridge University
Press), though its place in the standard textbook (Ewens,
2004, ibid.) reveals the widespread view among mathemat-
ical population geneticists. They had held for many decades
an extremely dim view of the fundamental theorem itself
(e.g. Charlesworth, 1970, ibid.; Karlin and Feldman, 1970,
Theor. Pop. Biol. 7, 364–398; Karlin, 1975, Theor. Pop. Biol.
1, 39–71), though some showed very little sign of having
read the original. Geneticists began to come to terms with the
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394       EDITORIAL
theorem in the 1980s, and it is still controversial—see Ewens
and Lessard (2015, Theor. Pop. Biol. 104, 59–67) and Grafen
(2018, J. Theor. Biol. 456, 175–189) for the latest news and
for references to the history.
The eclipse of the theorem mattered because biology was
a very broad subject, with theory and applications, and with
molecules, cells, organisms and communities. Holding it
all together requires general principles, and the fundamen-
tal theorem touched more parts of biology than any other.
Fisher himself (1930, ibid, p37) likened the theorem to the
Second Law of Thermodynamics and wrote “It is not a little
instructive that so similar a law should hold the supreme po-
sition among the biological sciences.” This view has not been
widely shared, but consider the remarks in an acceptance lec-
ture of a Nobel Prize in chemistry, which begin by referring
to an inequality involving the change in entropy over time:
The inequality in eq. 3, which does not involve
the total differentiation of a function, does not
in general permit one to define a Lyapunov
function. Before we come back to this ques-
tion, I should emphasize that 150 years after its
formulation the second law of thermodynam-
ics still appears to be more a program than a
well‐defined theory in the usual sense, as noth-
ing precise (except the sign) is said about the
S production. Even the range of validity of this
inequality is left unspecified. (Prigogine, 1978,
Science 201, 777–785, page 778)
The significant point here is the realistic appreciation of
the true role of a foundational principle. It must capture a
very basic and important idea with a fruitful way of look-
ing at the subject, and be capable of absorbing further intel-
lectual developments. Fisher had called in his 1930 preface
for a body of mathematical work in biology to match that
in physics, presumably mindful that physics is a very broad
subject that is bound together by standard theoretical nota-
tions and results that are part of the professional training of
all physicists. Biology still lacks any similar body of didac-
tic material: the fundamental theorem is in my view still the
place to start.
I end with two reflections. The centrality of applied work
in the study of natural selection began with its invention by
Darwin, for whom the breeding of pigeons and cattle was a
central inspiration. It continued with Fisher, whose invention
of reproductive value in 1927 came from work on an empiri-
cal life table for humans. And Robertson (1966, Anim. Prod.
8, 95–108) introduced his “secondary theorem of natural se-
lection” while writing about the culling process in cattle. The
high‐flying theoretical imagination benefits from concentra-
tion on cold hard facts.
Second, the fundamental theorem exhibits the scientific
contribution of Fisher and of his 1918 paper. The very term
“variance” was introduced in the 1918 paper, and Fisher could
understandably have felt he owned natural selection in a very
special way when a variance component turned up in the fun-
damental theorem. We should be aiming to catch up on lost
time by embracing Fisher’s result with the same enthusiasm!
Alan Grafen
Zoology Department and St John’s College, Oxford, UK
Email: alan.grafen@sjc.ox.ac.uk